Nematode Infection Patterns in a Neotropical Lizard Species from an Insular Mountain Habitat in Brazil

Home , Brasiliscincus, Plica plica, Tropidurus torquatus

Journal of Helminthology (2017) 91, 578–582 doi:10.1017/S0022149X16000754 © Cambridge University Press 2016

Nematode infection patterns in a Neotropical lizard species from an insular mountain habitat in Brazil

A.B.H.P. Václav1,3, L.A. Anjos2, M.S. Queiróz2, L.B. Nascimento3 and C.A.B. Galdino3* 1PET Biologia PUC Minas – MEC/SESu, Pontifícia Universidade Católica de Minas Gerais, 30535-901, Belo Horizonte, Brazil: 2Departamento de Biologia e Zootecnia, Laboratório de Parasitologia e Zoologia, UNESP, Universidade Estadual Paulista, FEIS, Passeio Monção 226, CEP 15385-000, Ilha Solteira, Brazil: 3Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, 30535-610, Belo Horizonte, Brazil (Received 12 July 2016; Accepted 27 September 2016; First published online 28 October 2016)

Abstract

Neotropical lizards are known to harbour rich nematode parasite faunas; however, knowledge of the diversity and patterns of infection are still lacking for many species. This is true for the genus Tropidurus, in which data on patterns of parasitism are known for only approximately 11 of its 30 species. We show that the nematode fauna associated with a population of Tropidurus montanus is composed of three species of host-generalist parasites with high overall prevalence. Male and female lizards did not differ in infection pattern and there was no relationship between host body size and intensity of infection for the most prevalent parasite species. Nevertheless, overall prevalence changed seasonally, with a higher proportion of parasitized individuals being found in the dry period than in the rainy period. We discuss our findings in the context of diet patterns of T. montanus, which we suggest may explain the similarities in prevalence and intensity of infection between the sexes. In addition, seasonal changes in diet are considered to be related to the observed differences in prevalence between dry and rainy periods.

Introduction variation in rainfall, which can, in turn, result in seasonal patterns of infection. Lizards are ectotherms, thus adjusting The major climatic factor influencing ecological systems their activity patterns and behaviours according to environ- in the Neotropics is seasonal variation between dry and mental conditions (e.g. Hatano et al., 2001;Filogonioet al., rainy periods. Changes in the amount of rain and in dur- 2010), and so patterns of helminth infection can be expected ation of the rainy period can affect patterns of infection to vary seasonally as well, reflecting the behavioural adjust- spread and persistence (see Altizer et al., 2006). Therefore, ments of these hosts (Ribas et al., 1995; Vrcibradic et al., parasitic interactions involving Neotropical species are ex- 1999; Pereira et al., 2012;Britoet al., 2014). pected to change over time in response to periodic Lizards are important components of the life cycle of many species of helminths, serving as definitive or intermediate hosts (e.g. Ávila & Silva, 2010). The helminth *E-mail: [email protected] fauna that parasitizes lizards is diverse and with varied All authors consented to participation in the study and agreed patterns of infection. In this sense, helminth richness can upon the content of the article. vary geographically among populations (Brito et al.,

Downloaded from https://www.cambridge.org/core. UNESP-Universidade Estadual Paulista, on 29 May 2019 at 17:00:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0022149X16000754 Nematode infection patterns in a Neotropical lizard 579

2014; Galdino et al., 2014), and changes in the composition Post-mortem examinations of the body cavity, digestive of component communities can be unrelated to geograph- tract, liver and lungs were undertaken using a stereomicro- ical distance among populations (Bezerra et al., 2016). scope. Nematodes were cleared with Aman’slactophenol Additionally, some studies have shown divergent results (Andrade, 2000) and analysed using a computerized sys- when considering whether infection rates and parasite tem for image analysis LAS 5.0 (Leica Application Suite), loads of helminths vary between sexes, or whether para- adapted to a DM 2500-Leica microscope with a differential site load is related to host body size. Hence, information interference contrast system (Leica, Wetzlar, Germany). All is still needed for a more complete understanding of the the parasitological terms used followed Bush et al.(1997). epidemiological and ecological patterns of helminth infec- Worms were deposited in the helminthological collection tion in lizards. of the Instituto de Biociências de Botucatu, Universidade The genus Tropidurus is speciose, with 30 species (Uetz Estadual Paulista (species batches: CHIBB 7861; CHIBB &Hošek, 2016). The genus harbours a rich helminth fauna 7862; CHIBB 7863), Botucatu, Brazil. with nearly 30 different parasite species and with compo- Differences between the sexes in overall helminth nent communities hosting from 3 to 21 species (Ávila & prevalence were tested by using the binomial test for Silva, 2010; Anjos et al., 2012). Recently, there have been each of the periods (rainy and dry). The binomial test efforts to uncover the diversity and patterns of helminth was also used to test for differences in prevalence between infection of species of Tropidurus (e.g. Tropidurus itambere, the two periods, considering all individuals in a period re- Ávila et al., 2011; T. hygomi and T. psammonastes, Lambertz gardless of sex. To evaluate the effects of period (dry and et al., 2012; T. spinulosus, Lunaschi et al., 2012; T. torquatus, rainy) and sex on the overall intensity of helminth infec- Pereira et al., 2012; T. oreadicus, Santos et al., 2013; tion we used a two-way analysis of variance (ANOVA). T. hispidus and T. semitaeniatus, Brito et al., 2014); however, Effects of body size on intensity of infection were evalu- parasitological data are missing for approximately 60% of ated for the helminth species with higher prevalence by the species of the genus. conducting a Generalized Linear Mixed Models analysis The occurrence of the lizard T. montanus is restricted to considering each individual as a random effect variable. the rocky outcrop formations of the mountaintop habitats In addition, we used a one-factor permutation test to of the Serra do Espinhaço (Espinhaço mountain range) in evaluate the effect of period on infection intensity of the South America (Rodrigues, 1987). To the best of our more prevalent helminth species (Hothorn et al., 2008). knowledge, information on parasitism of this species by helminths is lacking. The aim of the present study was to describe the helminth species composition and infec- Results tion levels in the Neotropical lizard T. montanus, relative to seasonality, host sex and size. The helminth component community of T. montanus (n = 80) was found to be composed of three species: Parapharyngodon alvarengai Freitas, 1957 (Pharyngodoni- Materials and methods dae) (prevalence = 59%; mean intensity of infection = 5.6 ± 5.1), found in both large and small intestines; Physaloptera We conducted the study in the rocky outcrop formation sp. Rudolphi, 1819 (Physalopteridae) (prevalence = 12%; at c.1460 m above mean sea level in the Serra da Piedade mean intensity of infection = 4.9 ± 8.2), found in the larval (Piedade mountain range; 19°49′S; 43°40′W), a branch of stage in the stomach and large intestine, and Strongyluris the Espinhaço Range, in the state of Minas Gerais, oscari Travassos, 1923 (Heterakidae) (prevalence = 44%; Brazil. High-elevation open habitats of the mountains mean intensity of infection = 6.0 ± 7.2) found in lungs, from eastern Brazil (which include the Espinhaço Range large and small intestines. Therefore, P. alvarengai and and related branches) are considered as isolated insular S. oscari were the most prevalent nematodes found para- environments that play a role in biogeographical sitizing individual lizards. Of the total of 80 lizards processes of plant and animal species (Chaves et al., sampled, 64 were parasitized by at least one species, re- 2015, Neves et al., 2016). The mean annual temperature sulting in an overall prevalence of 80%. Regarding infra- is 21°C and the mean annual rainfall averages 1650 mm. communities, 64% of lizards were parasitized by a The region experiences a marked distinction between single parasite species, while 30% of the hosts were para- rainy (from October to March) and dry (from April to sitized by two and 6% by three species. Nematode September) periods (Alvares et al., 2014). abundance averaged 7.4 ± 6.3. The intensities of infection Sampling of lizards took place during the rainy by P. alvarengai and by S. oscari were not related to host (December 2012) and dry months (June to August 2013). body size (P = 0.07, n = 52 and P = 0.60, n = 50, Lizards were sampled by performing visual encounter respectively). surveys throughout the period of activity of the species, We sampled 17 males and 20 females of T. montanus in and captured by noose or by shooting rubber bands. the rainy period and 21 males and 22 females in the dry Captured lizards were killed by lethal injection of sodium period. In the dry period, 95% of males and 100% of fe- thiopental, measured for body size (snout-to-vent length) males were found to harbour helminths, with no differ- with a Vernier caliper (nearest 0.1 mm), fixed and pre- ence in overall prevalence between the sexes (P = 0.98). served following standard procedures, and deposited in During the rainy period, 70% of males and 50% of females the herpetological collection of the Museu de Ciências were found to be parasitized and there was no difference Naturais of Pontifícia Universidade Católica de Minas in prevalence between males and females for the rainy Gerais (MCNR 4893–4934; 5114–5145; 5159–5174), Belo period (P = 0.34). The population of T. montanus had high- Horizonte, Brazil. er overall prevalence during the dry period (97%) than

during the rainy period (59%) (P < 0.001). The overall in- seems to hold true for lizards, with species-poor helminth tensity of helminth infection did not differ between sea- infracommunities being found on hosts from insular en- sons or between sexes (two-way ANOVA: F = 0.03, vironments (Dobson et al., 1992; Martin & Roca, 2005). P = 0.85). The intensity of infection by P. alvarengai and Therefore, the insular nature of the sampled area might S. oscari did not vary between dry and rainy periods (one- constrain the available pool of helminth species that can factor permutation test, Z = 1.52, P = 0.14 and Z = −1.18, infect individuals of T. montanus. P = 0.26, respectively). We found no intersexual difference in overall parasite prevalence. Intersexual differences in parasite prevalence are generally related to distinct social roles of male and fe- Discussion male lizards, which in turn are associated with unequal blood hormone levels (Fuxjager et al., 2011; see also The nematode community parasitizing T. montanus was Anjos et al., 2012). Males of T. montanus use larger home composed of three species. Of these, the nematode ranges than females (Galdino et al., in prep.), which is a P. alvarengai (Pharyngodonidae) is known to infect other proxy for different social roles between the sexes. Thus, lizard species, including Ameiva ameiva (Padilha & one might expect that the use of larger areas by males Duarte, 1979), Trachylepis atlantica (Ávila & Silva, 2010), might expose them to greater chances of infection, at Hemidactylus agrius (Anjos et al., 2011), Urosaurus auricula- least by P. alvarengai, a monoxenous parasite species. tus (Goldberg & Bursey, 2012), Tropidurus hispidus Therefore, our results cannot be explained by the different (Brito et al., 2014; Galdino et al., 2014) and Tropidurus social role and/or space use of males and females of T. semitaeniatus (Bezerra et al., 2015). The nematode S. oscari, montanus. Concerning heteroxenous parasites, we re- is considered to be a host generalist (i.e. parasitizing many garded the similarities in prevalence between the sexes host species), with a heteroxenic life cycle with arthropods as being due to a broad diet overlap between males and as intermediate hosts (Barreto-Lima & Anjos, 2014), and is females, as shown by Kiefer (1998). Therefore, the similar- a common parasite of lizards of the genus Tropidurus ity in overall prevalence of S. oscari between the sexes (Ávila & Silva, 2010), having been found in T. guarani, might be related to males and females having the same T. spinulosus, T. torquatus, T. melanopleurus and T. hispidus dietary patterns. (Bursey & Goldberg, 2004; Ávila & Silva, 2010; Brito et al., We did not find any relationship between T. montanus 2014). Moreover, S. oscari is known to infect lizards of body size and intensity of infection of either P. alvarengai other taxa, such as Ameiva ameiva, Anolis fuscoauratus, or S. oscari. It is argued that hosts with a larger body size A. punctatus, A. transversalis, Enyalius bilineatus, would provide more space for helminths to colonize, Eurolophosaurus nanuzae, Brasiliscincus agilis, Plica plica thereby leading to a positive relationship between the and P. umbra (Fontes et al., 2003; Ávila & Silva, 2010; two variables (Poulin, 1997; Ribas et al., 1998). It is also Barreto-Lima & Anjos, 2014). The third parasite species suggested that changes in infection intensity with size found, Physaloptera sp., is known to parasitize A. ameiva, will be related to ontogenetic changes in diet (Fontes Glaucomastix littoralis, Ameivula ocellifera, H. mabouia, et al., 2003). In the case of T. montanus, young and adult B. agilis, Psychosaura macrorhyncha, Polychrus acutirostris, lizards have similar diets, and so the non-relationship be- Tropidurus etheridgei, T. torquatus, T. hispidus, Salvator tween intensity of infection and lizard body size might be meriane and Tupinambis teguixin (Ávila & Silva, 2010; associated with ontogenetic conservatism in diet, which in Ávila et al., 2012; Pereira et al., 2012). Therefore, the com- turn might expose both young and adults to the same ponent community of helminths parasitizing the lizard chances of infection. A relationship between lizard body T. montanus can be considered to be comprised of host size and intensity of infection was not found for other spe- generalist parasites, and our record extends hosts species cies of lizards (e.g. T. torquatus and Brasiliscincus (former for P. alvarengai and S. oscari. Mabuya) agilis (Van Sluys et al., 1997), T. hispidus The component community of parasites of T. montanus (Galdino et al., 2014) and T. semitaeniatus (Bezerra et al., is species poor when compared to those found for other 2015)), suggesting that, in general, there is no trend be- species of the genus (e.g. T. torquatus (Pereira et al., tween body size and intensity of infection for lizards. 2012), T. hispidus (Brito et al., 2014; Galdino et al., 2014) Our results indicated that some patterns of helminth in- and T. semitaeniatus (Brito et al., 2014, Bezerra et al., fection in lizards may vary seasonally. We found that the 2015)). The high-elevation formations of the mountains proportion of infected hosts was higher during the dry from eastern Brazil, such as the rocky outcrops from the period than during the rainy period. Seasonal variation highlands of the Espinhaço Range, are considered to be in helminth infection patterns has also been found for an archipelago of isolated insular mountaintop habitats the Neotropical T. torquatus, with larger overall intensity (e.g. Chaves et al., 2015). Therefore, the insularity of the of infection during the dry period (Pereira et al., 2012). mountaintop rocky outcrops of the Serra da Piedade is re- In the case of T. torquatus, Pereira et al.(2012) suggested markable as this mountain is apart from the main that interseasonal differences in overall intensity of infec- Espinhaço Mountain Range where T. montanus is distrib- tion might be related to the consumption of a plant species uted. The helminth fauna of hosts inhabiting insular with anthelmintic compounds. Although T. montanus in- environments can be expected to be poorer than those creases its consumption of plant material during the dry parasitizing hosts on the mainland (e.g. Dobson et al., period (Kiefer, 1998), we are not able to relate the ob- 1992). For example, the pattern of helminths infecting ro- served seasonal variation in overall helminth intensity dir- dent species differed between insular and continental po- ectly to plant ingestion. Alternatively, as the diet pulations, with insular populations having lower composition of T. montanus varies seasonally (Kiefer, helminth richness (Kuhnen et al., 2012). The same pattern 1998), the observed change in overall prevalence in our

study might be related to seasonal changes in the types of Ávila, R.W. & Silva, R. (2010) Checklist of helminths from ingested food items. lizards and amphisbaenians (Reptilia, Squamata) of South America. Journal of Venomous Animals and Toxins Including Tropical Diseases 16, 543–572. Acknowledgements Ávila, R.W., Cardoso, M.W., Oda, F.H. & Silva, R.J. We are grateful to the administrative staff of Santuário (2011) Helminths from lizards (Reptilia: Squamata) at Estadual Nossa Senhora da Piedade for the permit to the Cerrado of Goiás State, Brazil. Comparative – work in the area. We thank M.J. Goulart, C.M. de Parasitology 78, 120 128. Oliveira, L.K. Pereira, L.H.A. Glauss and C.C. Lisboa for Ávila, R.W., Anjos, L.A., Ribeiro, S.C., Morais, D.H., their kind help during the fieldwork. We thank E. Wild Silva, R.J. & Almeida, W.O. (2012) Nematodes of li- for the English language review. C.A.B.G. and L.B.N. zards (Reptilia: Squamata) from Caatinga Biome, – thank Instituto Chico Mendes (ICMBio) for the permit to Northeastern Brazil. Comparative Parasitology 79,56 63. collect the animals. Barreto-Lima, A.F. & Anjos, L.A. (2014) Occurrence of Strongyluris oscari (Nematoda; Heterakidae) in Enyalius bilineatus (Squamata: Leiosauridae) from the Brazilian Financial support Atlantic Forest. Herpetology Notes 7, 455–456. A.B.H.P.V. thanks the Programa de Educação Tutorial/ Bezerra, C.H., Ávila, R.W., Passos, D.C., Zanchi-Silva, D. Ministério da Educação/Secretaria de Ensino Superior for & Galdino, C.B.A. (2015) Levels of helminth infection grant funding. L.A.A. is thankful to Fundação de Amparo in the flat lizard Tropidurus semitaeniatus from north- à Pesquisa do Estado de São Paulo (FAPESP, process no. eastern Brazil. Journal of Helminthology. doi:10.1017/ 2012/20978-2) for grant funding. L.B.N. thanks S0022149X15000826. Fundação de Amparo à Pesquisa do Estado de Minas Bezerra, C.H., Pinheiro, L.T., Melo, G.C., Zanchi-Silva, Gerais (FAPEMIG, processes CRA APQ-00683-12 and D., Queiroz, M.S., Anjos, L.A., Harris, D. & CRA APQ-02067-14); Fundo de Incentivo à Pesquisa Borges-Nojosa, M. (2016) Assessing the influence of (FIP/PUC Minas) and the Conselho Nacional de geographic distance in parasite communities of an Desenvolvimento Científico e Tecnológico (CNPq, process exotic lizard. Acta Parasitologica 61, 136–143. 479457/2012-3) for financial support. Brito, S.V., Ferreira, F.S., Ribeiro, S.C., Anjos, L.A., Almeida, W.O., Mesquita, D.O. & Vasconcellos, A. (2014) Spatial–temporal variation of parasites in Conflict of interest Cnemidophorus ocellifer (Teiidae) and Tropidurus hispi- None. dus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in northeastern Brazil. Parasitology Research 113, 1163–1169. Ethical standards Bursey, C.R. & Goldberg, S.R. (2004) Helminths of We followed the Guidelines for the Euthanasia of Animals Tropidurus guarani (Sauria: Tropiduridae) from (2013) of the American Veterinary Medical Association for Paraguay. Comparative Parasitology 71, 203–207. euthanizing the lizards. The Instituto Chico Mendes de Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. Conservação da Biodiversidade issued the permits (1997) Parasitology meets ecology on its own terms: (SisBio 35541 and 37266-3) to collect the animals. Margolis et al. revisited. Journal of Parasitology 83, 575– 583. References Chaves, A.V., Freitas, G.H.S., Vasconcelos, M.F. & Santos, F.R. (2015) Biogeographic patterns, origin and Altizer, S., Dobson, A., Hosseini, P., Hudson, P., speciation of the endemic birds from eastern Brazilian Pascual, M. & Rohani, P. (2006) Seasonality and the mountaintops: a review. Systematics and Biodiversity 13, dynamics of infectious diseases. Ecology Letters 9, 467– 1–16. 484. Dobson, A.P., Pacala, S.W., Roughgarden, J.D., Carper, Alvares, C.A., Stape, J.L., Sentelhas, P.C., Moraes, J.L.G. E.R. & Harris, E.A. (1992) The parasites of Anolis li- & Sparovek, G. (2014) Koppen’s climate classification zards in the northern Lesser Antilles. I. Patterns of map for Brazil. Meteorologische Zeitschrift 22, 711–728. distribution and abundance. Oecologia 91, 110–117. Andrade, C. (2000) Meios e soluções comumente empregados Filogonio, R., Del Lama, F.S., Machado, L.L., Drumond, em laboratórios. 1st edn. 353 pp. Seropédica, Bazil, M., Zanon, I., Mezzetti, N.A. & Galdino, C.A.B. UFRRJ. (2010) Daily activity and microhabitat use of sympatric Anjos, L.A., Bezerra, C.H., Passos, D.C., Zanchi, D. & lizards from Serra do Cipó, southeastern Brazil. Galdino, C.A.B. (2011) Helminth fauna of two gecko Iheringia, Série Zoologia 100, 336–340. lizards, Hemidactylus agrius and Lygodactylus klugei Fontes, A.F., Vicente, J.J., Kiefer, M.C. & Van Sluys, M. (Gekkonidae), from caatinga biome, northeastern (2003) Parasitism by helminths in Eurolophosaurus na- Brazil. Neotropical Helminthology 5, 285–290. nuzae (Lacertilia: Tropiduridae) in an area of rocky Anjos, L.A., Ávila, R.W., Ribeiro, S.C., Almeida, W.O. & outcrops in Minas Gerais State, Southeastern Brazil. Silva, R.J. (2012) Gastrointestinal nematodes of the Journal of Herpetology 37, 736–741. lizard Tropidurus hispidus (Squamata: Tropiduridae) Fuxjager, M.J., Foufopoulos, J., Diaz-Uriarte, R. & from a semi-arid region of north-eastern Brazil. Journal Marler, C.A. (2011) Functionally opposing effects of of Helminthology 87, 443–449. testosterone on two different types of parasite:

implications for the immunocompetence handicap Mountains: land conversion and ecosystem services. hypothesis. Functional Ecology 25, 132–138. pp. 501–526 in Fernandes, G.W. (Ed.) Ecology and con- Galdino, C.A.B., Ávila, R.W., Bezerra, C.H., Passos, D. servation of mountaintop grasslands in Brazil. C., Melo, G.C. & Zanchi-Silva, D. (2014) Helminth Switzerland, Springer. infection patterns in a lizard (Tropidurus hispidus) Padilha, T.N. & Duarte, M.J.F. (1979) Ocorrência de population from a semiarid Neotropical area: associa- Parapharyngodon alvarengai Freitas, 1957, em Ameiva tions between female reproductive allocation and ameiva (L.) no estado do Rio de Janeiro (Nematoda, parasite loads. Journal of Parasitology 100, 864–867. Oxyuroidea). Atas da Sociedade de Biologia do Rio de Goldberg, S.R. & Bursey, C.R. (2012) Endohelminths of Janeiro 20,21–22. the Socorro Island Tree Lizard, Urosaurus auriculatus Pereira, F.B., Sousa, B.M. & Lima, S.S. (2012) Helminth (Squamata: Phrynosomatidae), from Colima, Mexico. community structure of Tropidurus torquatus Comparative Parasitology 79, 269–274. (Squamata: Tropiduridae) in a rocky outcrop area of Hatano, F.H., Vrcibradic, D., Galdino, C.A.B., Minas Gerais state, southeastern Brazil. Journal of Cunha-Barros, M., Rocha, C.F.D & Van Sluys, M. Parasitology 98,6–10. (2001) Thermal ecology and activity patterns of the Poulin, R. (1997) Species richness of parasite assemblages: lizard community of the restinga of Jurubatiba, Macaé, evolution and patterns. Annual Review in Ecology and RJ. Revista Brasileira de Biologia 61, 287–294. Systematics 28, 341–358. Hothorn, T., Hornik, K., van de Wiel, M.A. & Zeileis, A. Ribas, S.C., Rocha, C.F.D., Teixeira-Filho, P.F. & (2008) Implementing a class of permutation tests: the Vicente, J.J. (1995) Helminths (Nematoda) of the lizard Coin package. Journal of Statistical Software 28,1–23. Cnemidophorus ocellifer (Sauria: Teiidae): assessing the Kiefer, M.C. (1998) Dieta, modo de forrageamentoe uso effect of rainfall, body size and sex in the nematode do microhábitat em duas espécies simpátricas de infection rates. Journal of Brazilian Association for the Tropidurus (Sauria, Tropiduridae) na Serra do Cipó, Advancement of Science 47,88–91. Minas Gerais. Master’s Dissertation, UNICAMP, Ribas, S.C., Rocha, C.F.D., Teixeira-Filho, P.F. & Campinas, Brazil. Vicente, J.J. (1998) Nematode infection in two sym- Kuhnen, V.V., Graipel, M.E. & Pinto, C.J.C. (2012) patric lizards (Tropidurus torquatus and Ameiva ameiva) Differences in richness and composition of gastro- with different foraging tactics. Amphibia–Reptilia 19, intestinal parasites of small rodents (Cricetidae, 323–330. Rodentia) in a continental and insular area of the Rodrigues, M.T. (1987) Sistematica, ecologia e zoogeo- Atlantic Forest in Santa Catarina state, Brazil. Brazilian grafia dos Tropidurus do grupo torquatus ao sul do Rio Journal of Biology 72, 563–567. Amazonas (Sauria, Iguanidae). Arquivos de Zoologia 31, Lambertz, M., Kohlsdorf, T., Perry, S.F., Ávila, R.W. & 105–230. Silva, R.J. (2012) First assessment of the endoparasitic Santos, J.N., Melo, F.T.V., Nazaré, L.C., Furtado, A.P. & nematode fauna of four psammophilous species of Giese, E.G. (2013) Strongyluris amazonicus n. sp. Tropiduridae (Squamata: Iguania) endemic to north- (Nematoda: Heterakidae): a parasite of Tropidurus eastern Brazil. Acta Herpetologica 7, 315–323. oreadicus from the Brazilian Amazon. Acta Tropica 128, Lunaschi, L.I., Lamas, M.F. & Drago, F.B. (2012) A new 96–102. species of Mathevotaenia (Cestoda, Anoplocephalidae) Uetz, P. & Hošek, J. (Eds). (2016) The reptile database. parasitizing Tropidurus spinulosus (Reptilia, Squamata) Available at http://www.reptile-database.org (ac- from northeastern Argentina. Revista Mexicana de cessed 20 June 2016). Biodiversidad 83, 583–590. Van Sluys, M., Rocha, C.F.D., Bergallo, H.G., Vrcibradic, Martin, J.E. & Roca, V. (2005) Helminths of the Atlantic D. & Ribas, S.C. (1997) Nematode infection in three lizard, Gallotia atlantica (Reptilia, Lacertidae), in the sympatric lizards in an isolated fragment of restinga Canary Islands (Eastern Atlantic): composition and habitat in southeastern Brazil. Amphibia–Reptilia 18, structure of component communities. Acta 442–446. Parasitologica 50,85–89. Vrcibradic, D., Rocha, C.F.D., Ribas, S.C. & Vicente, J.J. Neves, A.C.O., Barbieri, A.F., Pacheco, A.A., Resende, F. (1999) Nematodes infecting the skink Mabuya frenata in M., Braga, R.F., Azevedo, A.A. & Fernandes, G.W. Valinhos, São Paulo State, southeastern Brazil. (2016) The human dimension in the Espinhaço Amphibia–Reptilia 20, 333–339.